Skip to main content
NCBI home page
Annals of Botany logoLink to Annals of Botany
. 2008 Oct 24;103(1):87–94. doi: 10.1093/aob/mcn209

Acclimation of nitrogen uptake capacity of rice to elevated atmospheric CO2 concentration

Hiroyuki Shimono 1,*, James A Bunce 2
PMCID: PMC2707285  PMID: 18952623

Abstract

Background and Aims

Nitrogen (N) is a major factor affecting yield gain of crops under elevated atmospheric carbon dioxide concentrations [CO2]. It is well established that elevated [CO2] increases root mass, but there are inconsistent reports on the effects on N uptake capacity per root mass. In the present study, it was hypothesized that the responses of N uptake capacity would change with the duration of exposure to elevated [CO2].

Methods

The hypothesis was tested by measuring N uptake capacity in rice plants exposed to long-term and short-term [CO2] treatments at different growth stages in plants grown under non-limiting N conditions in hydroponic culture. Seasonal changes in photosynthesis rate and transpiration rate were also measured.

Key Results

In the long-term [CO2] study, leaf photosynthetic responses to intercellular CO2 concentration (Ci) were not affected by elevated [CO2] before the heading stage, but the initial slope in this response was decreased by elevated [CO2] at the grain-filling stage. Nitrate and ammonium uptake capacities per root dry weight were not affected by elevated [CO2] at panicle initiation, but thereafter they were reduced by elevated [CO2] by 31–41 % at the full heading and mid-ripening growth stages. In the short-term study (24 h exposures), elevated [CO2] enhanced nitrate and ammonium uptake capacities at the early vegetative growth stage, but elevated [CO2] decreased the uptake capacities at the mid-reproductive stage.

Conclusions

This study showed that N uptake capacity was downregulated under long-term exposure to elevated [CO2] and its response to elevated [CO2] varied greatly with growth stage.

Key words: Acclimation, elevated CO2, nitrogen uptake capacity, Oryza sativa, photosynthesis rate, rice, root development, transpiration rate

INTRODUCTION

The atmospheric carbon dioxide concentration [CO2] has been rising since the Industrial Revolution from 280 to 379 µmol mol−1, and is predicted to be double that in this century (IPCC, 2007). An increase of [CO2] can enhance leaf photosynthesis of C3 species, including rice and many other food crops, and can increase growth and grain yield (Kimball et al., 2002). Reported yield enhancement by elevated [CO2] varies widely due to different experimental methods, but canopy-level studies show it to be 10–20 % at +200 µmol mol−1 [CO2] under non-stress conditions (Kimball et al., 2002). This enhancement can be reduced under stress conditions such as low temperature (Okada et al., 2005; Shimono et al., 2008) and high temperature (Kim et al., 1996; Matsui et al., 1997). To keep pace with the increasing world food demand under future climates (United Nations, 2005), yield increases with high [CO2] could be important.

Nitrogen (N) uptake by roots is an important factor in achieving higher yields under elevated [CO2]. It is commonly accepted that higher amounts of N input lead to greater yield enhancement by elevated [CO2] (Rogers et al., 1996; Kimball et al., 2002; Kim et al., 2003), but the increment of yield enhancement by [CO2] per unit of N input became smaller with higher amounts of N input (Smart et al., 1998; Kimball et al., 2002; Kim et al., 2003). This might be attributed to limited sink capacities for absorbing N and C under higher amounts of N input (Rogers et al., 1996). However, considering the fact that plant N concentration on a dry weight basis at any N regime was reduced by elevated [CO2], N uptake may be a bottleneck for yield enhancement. If plants could absorb N to keep up with their dry weight increase, greater yield enhancement under elevated [CO2] might occur.

N uptake of roots is determined by the two factors root mass and capacity to take up N per unit of root. It is generally reported that elevated [CO2] increased root mass due to enhanced photosynthesis and growth (Kimball et al., 2002; Kim et al., 2003); a larger root mass could increase N uptake due to increased root surface coming into contact with soil nutrients. On the other hand, there is limited and conflicting information concerning the effects of elevated [CO2] on the N uptake capacity of roots per unit of root tissue. Elevated [CO2] increased N uptake capacity in red maple (1-year-old seedling; BassiriRad et al., 1999), did not alter the capacity of sorghum (40-d-old seedling) and sugar maple (1-year-old seedling; BassiriRad et al., 1999), and decreased the capacity of cottonwood trees (40-d-old seedling; McDonald et al., 2002), rice (80- to 100-d-old seedling; Morita et al., 2005) and loblolly and ponderosa pine (160-d-old seedling; BassiriRad et al., 1997). In the case of soybean, Delhon et al. (1996) reported a positive effect of elevated [CO2] on N uptake capacity using 20-d-old seedlings under growth chamber conditions, but BassiriRad et al. (1999) reported no effect of elevated [CO2] on N uptake capacity using 40-d-old seedlings in an open-top chamber experiment. Most of these studies relied on evaluations at a single growth stage, and there are limited studies concerning seasonal changes of N uptake capacity under long-term [CO2] elevation in spite of ample evidence of acclimation responses of several physiological characteristics involved in photosynthesis (reviewed by Moore et al., 1999), N allocation (e.g. Makino et al., 1997; Kim et al., 2003) and growth (e.g. Kim et al. 2003; Sakai et al., 2006). It is difficult to draw a clear picture of how N uptake capacity is affected by elevated [CO2].

N uptake capacity can be affected by various factors, most of which could also be affected by [CO2]. It is well known that elevated [CO2] increases photosynthesis and carbohydrate supply (Sasaki et al., 2005); the increased carbohydrate is expected to increase the N uptake capacity (Sasakawa and Yamamoto, 1978; Gastal and Saugier, 1989; Delhon et al., 1996; Lejay et al., 1999, 2003; Sehtiya and Goyal, 2000). Also, the enhanced photosynthesis and growth by elevated [CO2] promotes N utilization in plants, leading to a decrease in the concentration of N in plant tissues (Kimball et al., 2002). Since root N concentration is reported to be a signal for regulating N uptake capacity (Dluzniewska et al., 2006), the decreased N concentration in roots caused by elevated [CO2] might promote N uptake capacity. In contrast, elevated [CO2] generally reduces stomatal opening and transpiration (Kimball et al., 2002); the decreased transpiration stream caused by elevated [CO2] can decrease N uptake (McDonald et al., 2002). There are several reports of a close relationship between transpiration and N uptake (Delhon et al., 1995; Cerezo et al., 1999; Kiyomiya et al., 2001). Thus, elevated [CO2] could affect N uptake capacity both positively and negatively through variations in photosynthesis and transpiration. The present study examined the effects of elevated [CO2] on N uptake capacity in rice throughout the season in relation to the responses of photosynthesis, transpiration and growth. To help in interpreting the seasonal patterns, the effects of short-term elevation of [CO2] on N uptake at two growth stages were also examined for plants grown at ambient [CO2].

MATERIALS AND METHODS

Long-term [CO2] experiment

The rice cultivar ‘Akitakomachi’ (Oryza sativa L.) was grown hydroponicallly (not aerated) under two [CO2] conditions using two controlled environmental chambers (EGC Corp., Chagrin Falls, OH). The chambers were maintained at either 350 or 700 µmol mol−1 [CO2], and with a 12 h photoperiod [photosynthetically active radiation (PAR) of 650 µmol m−2 s−1 measured at pot height], 26/20 °C day/night temperature and 60 % relative humidity. Germinated seeds were sown on vermiculite held in plastic sieves (circular in shape with diameter 12 cm and 10 cm depth). After emergence (a week after sowing), the sieves were set into 4 L pots containing a complete nutrient solution (one plant per pot). The bottoms of the sieves were positioned above the nutrient solution, and all water and nutrient uptake occurred in roots which passed through the sieve into the nutrient solution. The nutrient solution contained 0·375 mm NH4Cl, 0·250 mm NH4H2PO4, 1·00 mm Ca(NO3)2·4H2O, 0·875 mm MgSO4·7H2O, 0·625 mm KCl, 1·00 mm KNO3, 0·250 mm K2SO4, 0·02 mm (NH4)6Mo7O24·4H2O, 5·15 mm H3BO3, 0·04 mm CuSO4·5H2O, 1·13 mm MnSO4·2H2O, 0·09 mm ZnSO4·7H2O and 26·9 mm Fe chelate (Sprint 330, Ciba-Geigy Corp., Greensboro, NC) with the pH adjusted to 5·0. The nutrient solution was made up from tap water. It provided 3·6 mm N (3·0 mm nitrate and 0·63 mm ammonium). The solution was refreshed and the pots were rotated inside the chamber once a week for the first month, twice a week for the next month and three times a week after that to supply enough nutrients and minimize error caused by locations. Each [CO2] chamber had 11 plants (one plant per pot). Note that in paddy fields, ammonium is abundant rather than nitrate, and the ammonium concentration is at most about 0·3 mm (Yamakawa et al., 2004).

Measurements of N uptake capacity, CO2 assimilation rate and dry weight were conducted at three growth stages [panicle initiation (PI), full heading (HD) and mid-ripening (RP)] for 3–4 plants per each [CO2]. At each stage, firstly N uptake capacity and plant transpiration were measured [PI = 53 days after sowing (DAS), HD = 96 DAS, RP = 119 DAS], then the photosynthesis rate was measured using a portable photosynthesis system (LI-6400, LI-COR, Lincoln, NE; PI = 55 DAS, HD = 98 DAS, RP = 125 DAS) and, finally, plants were harvested (PI = 59 DAS, HD = 101 DAS, RP = 133 DAS). The harvested plants were separated into green leaves, stem and culms, panicles (if present), roots and dead leaves, and dried for 72 h at 70 °C. The plant tissue samples were measured for N concentration using a CHN analyser (Perkin Elmer 2400, Series II CHNS/O Analyzer, Waltham, MA). Heading date, defined as the date when 50 % of productive tillers headed, was measured at 2 d intervals.

N uptake capacity was measured for 24 h using 2·0 L plastic beakers filled with 1·6 L of the nutrient solution described above. The volume and the concentration of nitrate and ammonium in the nutrient solution were measured at the beginning and at the end of the 24 h period using ion-specific electrodes (Cole-Palmer Inst. Co., Vernon Hill, IL). Electrodes were calibrated using five known concentrations of nitrate and ammonium solutions before the measurements. The reproducability was ±0·03 mm in the range from 1·1 to 6·3 mm for nitrate and ±0·13 mm in the range from 0·3 to 2·5 mm. N uptake capacity (NUC) was calculated from the following equation separately for nitrate and ammonium.

graphic file with name mcn20907.jpg 1

where Vinitial, Vfinal, cNinitial, cNfinal and RDW are the volume (V) and the concentration of nitrate or ammonium form (cN) at the start and the end of measurement, and the root dry weight that was in the nutrient solution (RDW), respectively. The reduction in the volume and the concentration without plants was very small [<1–2 % (v/v)], so this was not taken into account in the calculation. The transpiration rate was calculated from the volume change.

Short-term [CO2] experiment

The rice cultivar ‘Akitakomachi’ was hydroponically grown using a controlled environmental chamber with the same growth conditions as in the long-term [CO2] experiment, except for [CO2]. The chamber was maintained at a [CO2] of 350 µmol mol−1.

Plants were exposed to a 24 h treatment of two levels of [CO2] (350 or 700 µmol mol−1) at the early vegetative stage (46 and 48 DAS) and to three levels of [CO2] (200, 350 or 700 µmol mol−1) at the mid-reproductive stage (72–74 DAS). The experiment at the early vegetative stage was conducted using two independent growth chambers; six plants were moved from a control chamber to a treatment chamber at 700 µmol mol−1 at 46 DAS, and another six plants were moved to the treatment chamber at 350 µmol mol−1 at 48 DAS. The experiment at the mid-reproductive stage was conducted by using three independent chambers at 200, 350 or 700 µmol mol−1. A total of 12 plants were distributed into four groups (denoted as A, B, C and D) with three plants in the four replicate groups. Each group was exposed to a different [CO2] in a different order (at 72 DAS, group A, D = 200 µmol mol−1, C = 350 µmol mol−1, B = 700 µmol mol−1; at 73 DAS, group C = 200 µmol mol−1, A, B = 350 µmol mol−1, D = 700 µmol mol−1; at 74 DAS, group B = 200 µmol mol−1, D = 350 µmol mol−1, C, A = 700 µmol mol−1). Leaf area averaged 503 ± 24 cm2 per plant at the early vegetative stage and 1698 ± 102 cm2 per plant at the mid-reproductive stage.

Statistical analysis

For the long-term [CO2] study, statistical analysis was conducted by t-tests. For the short-term [CO2] study, statistical analysis was conducted for parameters at the early vegetative stage by t-tests using individual plants as replicates for the experiment (n = 4 or 6), and statistical analysis was conducted for parameters at the mid-reproductive stage by one-way analysis of variance, using the least significant difference test with P = 0·05 for separation of means of four replicates (= groups) as implemented by the SPSS for Windows 7·5J statistical software (SPSS, Inc., Chicago, IL). Regression analysis was conducted by comparing the residual variation about a common line with the sum of residual variations about individual lines (Mead et al., 2003). When the regressions were significantly different by this test, fitting parallel lines was tested by a comparison between the residual variation about parallel lines and the sum of residuals from fitting individual lines of different slope.

RESULTS

Long-term [CO2] experiment

Elevated [CO2] promoted heading date by only 1 d from 102 DAS at ambient [CO2] to 101 DAS at elevated [CO2]. Elevated [CO2] increased total dry weight and root dry weight, but the magnitude of the enhancement decreased with successive growth stages from 35 to 6 % for total dry weight and from 39 to 9 % for root dry weight (Fig. 1). Green leaf area was not affected by elevated [CO2] before the heading stage, but it was reduced by 17 % at the grain-filling stage (P < 0·05), indicating that elevated [CO2] promoted leaf senescence. Because elevated [CO2] reduced plant N concentration per dry weight at all stages (data not shown), elevated [CO2] did not increase total plant N content at any growth stage in spite of the fact that root system mass had been increased by elevated [CO2] (Fig. 1). The ratio of root dry weight to top dry weight was not affected by elevated [CO2].

Fig. 1.

Fig. 1.

Open in a new tab

Seasonal changes in total dry weight (including roots), root dry weight, green leaf area, total N content and ratio of root dry weight to top dry weight in rice plants exposed to long-term [CO2] treatments. Percentage changes due to elevated [CO2] are given. Bars indicate s.e. for 3–4 plants. An asterisk indicates significance at the 5 % level, and ns indicates not significantly different.

Leaf photosynthetic response to intercellular [CO2] (Ci; A–Ci response) was identical between the growth [CO2] treatments at both panicle initiation and heading (Fig. 2). However, at grain filling, the initial slope of plants grown under elevated [CO2] was lower than that of plants grown under ambient [CO2] although there was no difference in leaf photosynthesis at >1200 µmol mol−1 Ci.

Fig. 2.

Fig. 2.

Open in a new tab

Seasonal changes in leaf photosynthetic responses to intercellular CO2 concentration in rice plants exposed to long-term [CO2] treatments. Bars indicate s.e. for 3–4 plants.

Uptake capacities of nitrate and ammonium at panicle initiation based on root dry mass were not affected by elevated [CO2], but at the two later stages they were decreased by elevated [CO2] by about 40 % (Fig. 3). When the capacities were expressed based on root N, a similar pattern existed, but with somewhat smaller negative effects of elevated [CO2] (17 and 36 % at the two later stages, respectively) because root N concentration was reduced by elevated [CO2] (data not shown). Similar responses were observed for plant transpiration rate (Fig. 3). Positive relationships between total N (nitrate + ammonium) uptake capacity and transpiration rate were observed, and the relationships were independent at each growth stage (F4,14 = 153, P < 0·001; Fig. 4). The slopes in the regressions at the heading and grain-filling stages were identical, but not at the panicle initiation stage. Compared at the same transpiration rate, the N uptake capacity was greater for earlier growth stages than later growth stages.

Fig. 3.

Fig. 3.

Open in a new tab

Seasonal changes in nitrate and ammonium uptake capacities and transpiration rate in rice plants exposed to long-term [CO2] treatments. N uptake capacities and transpiration rate are expressed per unit of dry mass of root which reached through the sieve into the nutrient solution. Total N uptake capacity was expressed as the sum of nitrate and ammonium uptake capacities. Percentage changes due to elevated [CO2] are given. Bars indicate the s.e. for 3–4 plants. **, * and ns indicate the 1 %, 5 % and the not significantly different levels of significance, respectively.

Fig. 4.

Fig. 4.

Open in a new tab

The relationship between total N uptake capacity and plant transpiration rate of rice plants exposed to long-term [CO2] treatments. Total N uptake capacity was expressed as the sum of nitrate and ammonium uptake capacities. Correlation coefficients and regression equations are given. DAS, days after sowing. ***, * and ns indicate the 0·1 %, 5 % and the not significantly different levels of significance, respectively.

Short-term [CO2] experiment

Uptake capacities of N, for both ammonium and nitrate, increased with elevated [CO2] at the early vegetative stage (P < 0·05), but the capacities were decreased with elevated [CO2] at the mid-reproductive growth stage (P < 0·05; Fig. 5). However, at both the early vegetative and mid-reproductive stages, the transpiration rate was decreased by elevated [CO2].

Fig. 5.

Fig. 5.

Open in a new tab

Nitrate and ammonium uptake capacities and transpiration rates of rice plants exposed to short-term [CO2] treatments at two growth stages. N uptake capacities and transpiration rate are expressed per unit of dry mass of root which reached through the sieve into the nutrient solution. Total N uptake capacity was expressed as the sum of nitrate and ammonium uptake capacities. Bars indicate the s.e. of six individual plants at the early vegetative growth stage and of four averaged groups of plants at the mid-reproductive stage. The same letter indicates that mean values were not significantly different at the 5 % probability level.

There were close positive relationships between N uptake capacity and transpiration rates at the mid-reproductive growth stage over all levels of [CO2] (Fig. 6). However, at the early vegetative stage, the relationships were different between [CO2] (F2, 8 = 4·29, P < 0·05 using all data; F2, 6 = 69·6, P < 0·001 using data excluding one data point for each [CO2]). When including all data, significant relationships between N uptake capacity and transpiration rate could not be detected at either [CO2], but data excluding one data point for each [CO2] (circled in Fig. 6) showed significant and positive relationships between N uptake capacity and transpiration rate at each [CO2].

Fig. 6.

Fig. 6.

Open in a new tab

Relationships between total N uptake capacity and plant transpiration rate of rice plants exposed to short-term [CO2] treatments at different growth stages. Total N uptake capacity was expressed as the sum of nitrate and ammonium uptake capacities. Correlation coefficients and regression equations are given. ***, **, * and ns indicate the 0·1 %, 1 %, 5 % and the not significantly different levels of significance, respectively.

DISCUSSION

The present study showed that responses of uptake capacities of both ammonium and nitrate to elevated [CO2], estimated based on uptakes per unit root mass, changed with plant growth stage and/or duration of exposure to elevated [CO2]. This was evident in the long-term study by the lower capacities of N uptake at elevated [CO2] in the later growth stages, and in the short-term study by the contrasting responses of N uptake to elevated [CO2] at the two growth stages. The short-term effect of elevated [CO2] in the vegetative stage was an increase in N uptake capacities (Fig. 5), and this contrasts with the lack of increase in N uptake capacities at elevated [CO2] even at the earliest stage measured in the long-term study (Fig. 3), and the lack of increase in total N content per plant throughout the season despite greater root dry weight (Fig. 1). The contrast between the short-term and long-term responses suggested that acclimation of N uptake capacity to elevated [CO2] occurred in the early growth stages. However, the lower capacities at elevated [CO2] at the later growth stages in the long-term experiment (Fig. 3) were consistent with the decrease in N uptake at elevated [CO2] in the short-term experiment at the later growth stage (Fig. 5). Because the short-term [CO2] response for plants exposed to long-term [CO2] was not measured, it cannot be concluded from the present results that acclimation of N uptake to elevated [CO2] continued in the later growth stages. However, the lower capacities at elevated [CO2] at the later growth stages in the long-term experiment (Fig. 3) could have resulted from the acclimation response in addition to the direct effects of elevated [CO2] because it is generally observed that the acclimation of several physiological characteristics did not recover with prolonged duration of exposure to elevated [CO2] once plants had acclimated to elevated [CO2] (Makino et al., 1997; Moore et al., 1999; Kim et al., 2003; Sakai et al., 2006). The present study clearly demonstrated that growth stage and duration of exposure to elevated [CO2] were important in determining the patterns of N uptake in response to elevated [CO2].

Decreased transpiration might be one factor responsible for regulating N uptake capacity. In the long-term [CO2] study at each growth stages (Fig. 4) and in the short-term [CO2] study at the mid-reproductive stage (Fig. 6), there was a close positive correlation between N uptake capacity and transpiration rate over [CO2] environments. McDonald et al. (2002) exposed a 40-d-old cottonwood tree potted in soil to different [CO2] and humidity for 10 d, and demonstrated that the reduction in N uptake rate at elevated [CO2] resulted from a decreased transpiration rate in the short-term study at the early vegetative stage. Their experiment could not separate a direct effect of elevated [CO2] on N uptake capacity and an indirect effect of elevated [CO2] on N movement in the soil. The present study was conducted under hydroponic conditions, which excludes effects of nutrient movement in the soil, and showed that elevated [CO2] affected N uptake capacity.

However, in the short-term [CO2] experiment at the early growth stage (46–48 d old), the transpiration rate could not explain variations in N uptake capacity due to [CO2] (Fig. 6). At this stage, elevated [CO2] enhanced N uptake capacity even though elevated [CO2] significantly decreased the transpiration rate. Similar positive effects of elevated [CO2] on N uptake capacity using young seedlings have been reported in several previous studies (Sasakawa and Yamamoto, 1978; Gastal and Saugier, 1989; Delhon et al., 1996; Lejay et al., 1999, 2003; Sehtiya and Goyal, 2000). Those studies demonstrated a close correlation between an increased carbohydrate supply and the enhanced N uptake capacity under elevated [CO2]. Younger plants generally have higher N uptake capacity (e.g. high absolute N uptake capacity in Fig. 3 in the present study), and this might require more carbohydrate supply per unit of capacity than older plants, resulting in higher responsiveness to photosynthetic enhancement by elevated [CO2]. Similar factors might explain the different relationships between N uptake capacity and transpiration rate between different growth stages obtained in the long-term [CO2] study (Fig. 4). The present studies of short- and long-term [CO2] treatments suggested a system regulating N uptake capacity through transpiration and another process such as photosynthesis, and that the relative importance of the processes varied with growth stage.

The form of N provided (e.g. nitrate or ammonium) sometimes affects the responsiveness to [CO2]. For example, BassiriRad et al. (1997), comparing N uptake rates of loblolly and ponderosa pine, showed that in both species elevated [CO2] enhanced nitrate uptake but decreased ammonium uptake. Rice grown under flooding conditions is known to prefer ammonium rather than nitrate as an N source (Tanaka, 1970), and in normal paddy fields, ammonium rather than nitrate is the major N source (Yamakawa et al., 2004). In the present study, however, there was no difference in the response to [CO2] between ammonium and nitrate in either experiment (Figs 3 and 5). Note that plant biomass in the present experiment was substantially larger than under normal field conditions. The biomass at the mid-ripening stage in the long-term [CO2] study was 133 g per plant under ambient conditions in this experiment using the identical cultivar ‘Akitakomachi’ (Fig. 1) and this was 73 % greater than values observed in a field environment in Shizukuishi, Japan (39°38'N, 140°57'E) where the five-season average was 71 g per hill at harvest (three plants per hill) (1998–2000 and 2003–2004) (Kim et al., 2003; Shimono et al., 2008). The present experimental conditions were closer to optimal for rice growth than field conditions.

In conclusion, the present study clearly demonstrated that the effect of elevated [CO2] on the capacity of rice root systems to take up nitrate and ammonium ions changed with the stage of growth and showed acclimation to elevated [CO2].

ACKNOWLEDGMENTS

We are grateful to Dr Dennis Timlin for his excellent presentation about modelling the effects of N uptake that provided a hint for the present analysis. We thank Mrs Frances Caulfield for the maintenance of the growth chambers and plants, Dr Junko Sakurai, Dr Mari Murai, Dr Kensaku Suzuki and Dr Takami Hayashi, of the National Agricultural Research Center for Tohoku Region, Japan, for the information about environmental conditions for growing rice, and the anonymous reviewers for invaluable comments and suggestions. This study was supported by a research fellowship from the Japanese Society for the Promotion of Science for Young Scientists.

LITERATURE CITED

  1. BassiriRad H, Griffin KL, Reynolds JF, Strain BR. Changes in root NH4+ and NO3− absorption rates of loblolly and ponderosa pine in response to CO2 enrichment. Plant and Soil. 1997;190:1–9. [Google Scholar]
  2. BassiriRad H, Prior SA, Norby RJ, Rogers HH. A field method of determining NH4+ and NO3− uptake kinetics in intact roots: effects of CO2 enrichment on trees and crop species. Plant and Soil. 1999;217:195–204. [Google Scholar]
  3. Cerezo M, Garcia-Agustin P, Primo-Millo E. Influence of chloride and transpiration on net 15NO3− uptake rate by citrus roots. Annals of Botany. 1999;84:117–120. [Google Scholar]
  4. Delhon P, Gojon A, Tillard P, Passama L. Diurnal regulation of NO3− uptake in soybean plants II. Relationship with accumulation of NO3− and asparagine in the roots. Journal of Experimental Botany. 1995;46:1595–1602. [Google Scholar]
  5. Delhon P, Gojon A, Tillard P, Passama L. Diurnal regulation of NO3− uptake in soybean plants IV. Dependence on current photosynthesis and sugar availability to the roots. Journal of Experimental Botany. 1996;47:893–900. [Google Scholar]
  6. Dluzniewska P, Gessler A, Kopriva S, Strnad M, Novak O, Dietrich H, Rennenberg H. Exogenous supply of glutamine and active cytokinin to the roots reduces NO3 uptake rates in poplar. Plant, Cell and Environment. 2006;29:1284–1297. doi: 10.1111/j.1365-3040.2006.01507.x. [DOI] [PubMed] [Google Scholar]
  7. Gastal F, Saugier B. Relationships between nitrogen uptake and carbon assimilation in whole plants of tall fescue. Plant, Cell and Environment. 1989;12:407–418. [Google Scholar]
  8. IPCC. Summary for Policy makers. In: Solomon S, Qin SD, Manning M, et al., editors. Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press; 2007. pp. 1–18. [Google Scholar]
  9. Kiyomiya S, Nakanishi H, Uchida H, Tsuji A, Nishiyama S, Futatsubashi M, et al. Real time visualization of 13N-translocation in rice under different environmental conditions using positron emitting tracer imaging system. Plant Physiology. 2001;125:1743–1753. doi: 10.1104/pp.125.4.1743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kimball BA, Kobayashi K, Bindi M. Responses of agricultural crops to free-air CO2 enrichment. Advances in Agronomy. 2002;77:293–386. [PubMed] [Google Scholar]
  11. Kim HY, Horie T, Nakagawa H, Wada K. Effects of elevated CO2 concentration and high temperature on growth and yield of rice: II. The effect on yield and its components of Akihikari rice. Japanese Journal of Crop Science. 1996;65:644–651. (in Japanese with English abstract) [Google Scholar]
  12. Kim HY, Lieffering M, Kobayashi K, Okada M, Mitchell MW, Gumpertz M. Effects of free-air CO2 enrichment and nitrogen supply on the yield of temperate paddy rice crops. Field Crops Research. 2003;83:261–270. [Google Scholar]
  13. Lejay L, Tillard P, Lepetit M, Olive FD, Filleur S, Daniel-Vedele F, Gojon A. Molecular and functional regulation of two NO3 uptake systems by N- and C-status of Arabidopsis plants. The Plant Journal. 1999;18:509–519. doi: 10.1046/j.1365-313x.1999.00480.x. [DOI] [PubMed] [Google Scholar]
  14. Lejay L, Gansel X, Cerezo M, Tillard P, Muller C, Krapp A, et al. Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. The Plant Cell. 2003;15:2218–2232. doi: 10.1105/tpc.013516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Makino A, Harada M, Sato T, Nakano H, Mae T. Growth and N allocation in rice plants under CO2 enrichment. Plant Physiology. 1997;115:199–203. doi: 10.1104/pp.115.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Matsui T, Namuco OS, Ziska LH, Horie T. Effects of high temperature and CO2 concentration on spikelet sterility in indica rice. Field Crops Research. 1997;51:213–219. [Google Scholar]
  17. McDonald EP, Erickson JE, Kruger EL. Can decreased transpiration limit plant nitrogen acquisition in elevated CO2? Functional Plant Biology. 2002;29:1115–1120. doi: 10.1071/FP02007. [DOI] [PubMed] [Google Scholar]
  18. Mead R, Curnow RN, Hasted AM, Chatfield C, Zidek J, Lindsey J, Tanner M, editors. Statistical methods in agriculture and experimental biology. 3rd edn. London: Chapman & Hall; 2003. pp. 237–258. [Google Scholar]
  19. Moore BD, Cheng SH, Sims D, Seemann JR. The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant, Cell and Environment. 1999;22:567–582. [Google Scholar]
  20. Morita S, Sakaigaichi T, Abe J, Kobayashi K, Okada M, Shimono H, et al. Structure and function of rice root system under FACE condition. Journal of Agricultural Meteorology. 2005;60:961–964. [Google Scholar]
  21. Okada M, Shimono H, Yamakawa Y, Inoue M, Kobayashi K. Effects of elevated CO2 on floral sterility of rice plants caused by low temperature. Journal of Agricultural Meteorology. 2005;60:589–592. [Google Scholar]
  22. Rogers GS, Milham PJ, Gillings M, Conroy JP. Sink strength may be the key to growth and nitrogen responses in N-deficient wheat at elevated CO2. Australian Journal of Plant Physiology. 1996;23:253–264. [Google Scholar]
  23. Sakai H, Hasegawa T, Kobayashi K. Enhancement of rice canopy carbon gain by elevated CO2 is sensitive to growth stage and leaf nitrogen concentration. New Phytologist. 2006;170:321–332. doi: 10.1111/j.1469-8137.2006.01688.x. [DOI] [PubMed] [Google Scholar]
  24. Sasakawa H, Yamamoto Y. Comparison of the uptake of nitrate and ammonium by rice seedlings: influences of light, temperature, oxygen concentration, exogenous sucrose, and metabolic inhibitors. Plant Physiology. 1978;62:665–669. doi: 10.1104/pp.62.4.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sasaki H, Aoki N, Sakai H, Hara T, Uehara N, Ishimaru K, Kobayashi K. Effect of CO2 enrichment on the translocation and partitioning of carbon at the early grain-filling stage in rice (Oryza sativa L.) Plant Production Science. 2005;8:8–15. [Google Scholar]
  26. Sehtiya H, Goyal S. Comparative uptake of nitrate by intact seedlings of C3 (barley) and C4 (corn) plants: effect of light and exogenously supplied sucrose. Plant and Soil. 2000;227:185–190. [Google Scholar]
  27. Shimono H, Okada M, Yamakawa Y, Nakamura H, Kobayashi K, Hasegawa T. Rice yield enhancement by elevated CO2 is reduced in cool weather conditions. Global Change Biology. 2008;14:276–284. [Google Scholar]
  28. Smart DR, Ritchie K, Bloom AJ, Bugbee BB. Nitrogen balance for wheat canopies (Triticum aestivum cv. Veery 10) grown under elevated and ambient CO2 concentrations. Plant, Cell and Environment. 1998;21:753–763. doi: 10.1046/j.1365-3040.1998.00315.x. [DOI] [PubMed] [Google Scholar]
  29. Tanaka A. Ion exclusion from rice roots. Japnese Journal of Soil Science and Plant Nutrients. 1970;41:457–460. (in Japanese) [Google Scholar]
  30. United Nations. The 2004 world population prospects. Revision population database. 2005. (http://esa.un.org/unpp/ )
  31. Yamakawa Y, Saigusa M, Okada M, Kobayashi K. Nutrient uptake by rice and soil solution composition under atmospheric CO2 enrichment. Plant and Soil. 2004;259:367–372. [Google Scholar]

Articles from Annals of Botany are provided here courtesy of Oxford University Press

RESOURCES